Behav Ecol Sociobiol (2005) 59: 215–221 DOI 10.1007/s00265-005-0027-6
ORIGINAL ARTICLE
Tanja Schwander · Herv´e Rosset · Michel Chapuisat
Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors
Received: 7 April 2005 / Revised: 6 June 2005 / Accepted: 6 June 2005 / Published online: 29 July 2005 C Springer-Verlag 2005
Abstract Division of labour among workers is central to the organisation and ecological success of insect societies. If there is a genetic component to worker size, morphology or task preference, an increase in colony genetic diversity arising from the presence of multiple breeders per colony might improve division of labour. We studied the genetic basis of worker size and task preference in Formica selysi, an ant species that shows natural variation in the number of mates per queen and the number of queens per colony. Worker size had a heritable component in colonies headed by a doubly mated queen (h2 =0.26) and differed significantly among matrilines in multiple-queen colonies. However, higher levels of genetic diversity did not result in more polymorphic workers across single- or multiplequeen colonies. In addition, workers from multiple-queen colonies were consistently smaller and less polymorphic than workers from single-queen colonies. The relationship between task, body size and genetic lineage appeared to be complex. Foragers were significantly larger than broodtenders, which may provide energetic or ergonomic advantages to the colony. Task specialisation was also often associated with genetic lineage. However, genetic lineage and body size were often correlated with task independently of each other, suggesting that the allocation of workers to tasks is modulated by multiple factors. Overall, these results indicate that an increase in colony genetic diversity does not increase worker size polymorphism but might improve colony homeostasis. Keywords Size polymorphism . Heritability . Polyethism . Social insects . Formica selysi
Communicated by J. Heinze T. Schwander () · H. Rosset · M. Chapuisat Department of Ecology and Evolution, Biology Building, University of Lausanne, 1015 Lausanne, Switzerland e-mail:
[email protected] Tel.: +0041-21-692-41-81 Fax: +0041-21-692-41-65
Introduction Division of labour among workers is an important component of the organization of insect societies that largely contributes to their ecological success (Wilson 1971; Oster and Wilson 1978). Workers tend to specialise on tasks such as brood tending, foraging or colony defence (H¨olldobler and Wilson 1990). To optimize colony efficiency, an adequate number of workers has to be allocated to each task, which has raised considerable interest in the factors and mechanisms influencing the behavioural specialization of workers (Oster and Wilson 1978; Beshers and Fewell 2001). Task preference is often associated with morphological adaptations, particularly in ants (Oster and Wilson 1978; H¨olldobler and Wilson 1990). The association between phenotype and task is most pronounced in species with morphologically distinct worker castes (Wilson 1976; Wetterer 1999). However, some amount of phenotype-task matching is also commonly found in species where workers do not belong to distinct castes but differ in size (Wilson 1968; Oster and Wilson 1978; H¨olldobler and Wilson 1990; Waser 1998), and this association between task and morphology has been shown to result in an increased efficiency of workers (Wilson 1980; Franks 1985; Porter and Tschinkel 1985b). Two studies have documented a significant genetic component to worker size within colonies of ants (Fraser et al. 2000; Hughes et al. 2003). These findings are in accordance with the hypothesis that genetically more diverse colonies have more variable workers, and hence a more efficient division of labour (Crozier and Page 1985; Robinson 1992). However, the heritability of worker size was low in another study (Bargum et al. 2004), and the impact of a heritable component to worker size on colony efficiency will depend on the precise relationship between task specialization, genotype and size, as well as on the regulation of worker size distribution at the colony level. Task preference may also have a direct genetic basis, independently of size. In many species of bees, wasps and ants, workers from different maternal or paternal
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lineages tend to carry out different tasks (Stuart and Page 1991; Page et al. 1995). This genetic polyethism might come from genetic variation in the response thresholds to task-related stimuli, which can generate individual specialisation while retaining a flexible allocation of workers to tasks that permits to match the needs of the colony (Robinson 1992; Beshers and Fewell 2001; Page and Erber 2002). An increase in colony genetic diversity may therefore allow a more complete or more sensitive expression of the genetically-based division of labour, leading to a more efficient worker force (Crozier and Page 1985; Robinson 1992). In this study, we evaluate if higher colony genetic diversity increases worker size polymorphism and thus may improve division of labor. We first test whether worker size and task preference have a genetic component within colonies of Formica selysi, an ant species that shows natural variation in the number of mates per queen and the number of queens per colony. We then examine how genetic diversity and social structure affect worker size polymorphism at the colony level, and disentangle the relative effect of size and genotype on task specialisation.
Materials and methods Study population and sampling The study population of F. selysi is located along the river Rhˆone between Sierre and Susten in Switzerland. The social structure of 112 colonies had previously been determined by genotyping eight to 24 workers at nine microsatellite loci (Chapuisat et al. 2004). The majority of the colonies (57%) were headed by one singly mated queen, a few (6%) had one doubly mated queen and the remaining (37%) had multiple queens. Single-queen colonies and multiple-queen colonies have similar mating systems and are not genetically differentiated (Chapuisat et al. 2004). We selected 17 colonies headed by a singly mated queen (monogyne, M1), six colonies headed by a doubly mated queen (monogyne, M2) and 20 colonies with multiple queens (polygyne, P). All but one polygyne colonies had many queens per colony, with genetically-effective queen number ranging from 4.6 to 36.1. The remaining colony, which had three matrilines and a genetically-effective queen number of 1.4, will be referred to as oligogyne (O, colony 96). All selected colonies were more than 4 years old and had already produced winged queens or males. We estimated colony size (the number of workers per colony) with a capture–recapture method described in Sundstr¨om (1995). To compare worker polymorphism across colonies, we collected a random sample of at least 50 workers from each of the 43 colonies. These individuals were sampled early in the morning when most workers are just below the nest surface to warm up. To estimate the correlations between genetic lineage, task and size, we collected foragers and brood tenders in a sub-
sample of 32 colonies. These colonies (16 M1, 4 M2, 1 O, 11 P) were the ones that contained a lot of small brood at the time of collection. Foragers were collected in three pitfall traps placed at 40 cm from the nest entrances. Brood tenders were identified by placing many workers, brood and sandy nest material into a plastic box with a black paper roof in one corner. After 15 min, we collected brood tenders, which were the workers caring for the brood under the paper roof. All sampling took place between June and August 2002. Morphometrics Workers were measured to the nearest 0.001 mm using a stereomicroscope Nikon V-12 at a magnification of 50×. In a preliminary investigation, we took six body measures from a random sample of 120 workers from each of four colonies (two M1 and two P): head width (maximum width across the eyes), head height, thorax length, scape length, tibia and femur lengths of the hind-leg. All six measures covaried isometrically, with correlation coefficients ranging between 0.72 and 0.90. We therefore decided to use head width as a single estimate of size, because it is easy to measure and is commonly used as a dependent variable in studies of allometry (Wheeler 1991). The repeatability of the measure of head width was high. On average, repeated measures from 50 ants differed by only 0.04 mm (3% of the first measure) and were highly correlated (Pearson’s moment correlation: 0.92; t48 =15.84, p
